Ecological and genetic interactions between cyanobacteria and viruses in a low-oxygen mat community inferred through metagenomics and metatranscriptomics

Environmental Microbiology

Volumn 18, Issue 2, 2016, Pages 358-371

  Voorhies, Alexander A ^a   Eisenlord, Sarah D ^a   Marcus, Daniel N ^a   Duhaime, Melissa B ^a   Biddanda, Bopaiah A ^c   Cavalcoli, James D ^b   Dick, Gregory J ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c GRAND VALLEY STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OXYGEN; PHYCOBILISOME;

ARCHAEON; BACTERIAL GENOME; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CYANOBACTERIUM; DNA SEQUENCE; ECOLOGY; GENETICS; LAKE; METABOLISM; METAGENOMICS; MICROBIOLOGY; NUCLEOTIDE SEQUENCE; PHYCOBILISOME; PHYLOGENY; PLASMID; VIRUS; VIRUS GENOME;

ARCHAEA; BASE SEQUENCE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CYANOBACTERIA; ECOLOGY; GENOME, BACTERIAL; GENOME, VIRAL; LAKES; METAGENOMICS; OXYGEN; PHYCOBILISOMES; PHYLOGENY; PLASMIDS; SEQUENCE ANALYSIS, DNA; VIRUSES;

EID: 84959537486     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12756     Document Type: Article

References (84)

1. Allers, E., Moraru, C., Duhaime, M.B., Beneze, E., Solonenko, N., Barrero-Canosa, J., etal. (2013) Single-cell and population level viral infection dynamics revealed by phagefish, a method to visualize intracellular and free viruses. Environ Microbiol 15: 2306-2318.
2. Allwood, A.C., Walter, M.R., Kamber, B.S., Marshall, C.P., and Burch, I.W. (2006) Stromatolite reef from the Early Archaean era of Australia. Nature 441: 714-718.
3. Anantharaman, K., Duhaime, M.B., Breier, J.A., Wendt, K.A., Toner, B.M., and Dick, G.J. (2014) Sulfur oxidation genes in diverse deep-sea viruses. Science 344: 757-760.
4. Anderson, M.J. (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26: 32-46.
5. Andersson, A.F., and Banfield, J.F. (2008) Virus population dynamics and acquired virus resistance in natural microbial communities. Science 320: 1047-1050.
6. Avrani, S., Wurtzel, O., Sharon, I., Sorek, R., and Lindell, D. (2011) Genomic island variability facilitates prochlorococcus-virus coexistence. Nature 474: 604-608.
7. Banfield, J.F., and Young, M. (2009) Variety - the splice of life - in microbial communities. Science 326: 1198-1199.
8. Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., etal. (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315: 1709-1712.
9. Biomatters (2013) Geneious. In.
10. Bogorad, L. (1975) Phycobiliproteins and complementary chromatic adaptation. Annu Rev Plant Physiol Plant Mol Biol 26: 369-401.
11. Bolhuis, H., and Stal, L.J. (2011) Analysis of bacterial and archaeal diversity in coastal microbial mats using massive parallel 16s rRNA gene tag sequencing. ISME J 5: 1701-1712.
12. Breitbart, M., Thompson, L.R., Suttle, C.A., and Sullivan, M.B. (2007) Exploring the vast diversity of marine viruses. Oceanography 20: 135-139.
13. Cai, F., Axen, S.D., and Kerfeld, C.A. (2013) Evidence for the widespread distribution of CRISPR-cas system in the phylum Cyanobacteria. RNA Biol 10: 687-693.
14. Clarke, K., and Gorley, R.N. (2006) Primer v6: User Manual/Tutorial. Plymouth, UK: PRIMER-E.
15. Clarke, K.R. (1993) Nonparametric multivariate analyses of changes in community structure. Aust J Ecol 18: 117-143.
16. Collier, J.L., and Grossman, A.R. (1994) A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria. EMBO J 13: 1039-1047.
17. Dammeyer, T., Bagby, S.C., Sullivan, M.B., Chisholm, S.W., and Frankenberg-Dinkel, N. (2008) Efficient phage-mediated pigment biosynthesis in oceanic cyanobacteria. Curr Biol 18: 442-448.
18. Deng, L., Gregory, A., Yilmaz, S., Poulos, B.T., Hugenholtz, P., and Sullivan, M.B. (2012) Contrasting life strategies of viruses that infect photo- and heterotrophic bacteria, as revealed by viral tagging. Mbio 3: e00373-12.
19. Dick, G.J., Andersson, A.F., Baker, B.J., Simmons, S.L., Yelton, A.P., and Banfield, J.F. (2009) Community-wide analysis of microbial genome sequence signatures. Genome Biol 10: R85.
20. Emerson, J.B., Thomas, B.C., Andrade, K., Allen, E.E., Heidelberg, K.B., and Banfield, J.F. (2012) Dynamic viral populations in hypersaline systems as revealed by metagenomic assembly. Appl Environ Microbiol 78: 6309-6320.
21. Frias-Lopez, J., Shi, Y., Tyson, G.W., Coleman, M.L., Schuster, S.C., Chisholm, S.W., and DeLong, E.F. (2008) Microbial community gene expression in ocean surface waters. Proc Natl Acad Sci USA 105: 3805-3810.
22. Gao, E.B., Gui, J.F., and Zhang, Q.Y. (2012) A novel cyanophage with a cyanobacterial nonbleaching protein a gene in the genome. J Virol 86: 236-245.
23. Garcia-Heredia, I., Martin-Cuadrado, A.B., Mojica, F.J.M., Santos, F., Mira, A., Anton, J., and Rodriguez-Valera, F. (2012) Reconstructing viral genomes from the environment using fosmid clones: the case of haloviruses. PLoS ONE 7: e33802.
24. Garneau, J.E., Dupuis, M.E., Villion, M., Romero, D.A., Barrangou, R., Boyaval, P., etal. (2010) The CRISPR/cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468: 67-71.
25. Gilbert, J.A., Field, D., Huang, Y., Edwards, R., Li, W., Gilna, P., and Joint, I. (2008) Detection of large numbers of novel sequences in the metatranscriptomes of complex marine microbial communities. PLoS ONE 3: e3042.
26. Giovannoni, S., Temperton, B., and Zhao, Y.L. (2013) Sar11 viruses and defensive host strains reply. Nature 499: E4-E5.
27. Golubic, S., and Abed, R. (2010) Entophysalis mats as environmental regulators. In Microbial Mats: Modern and Ancient Microorganisms in Stratified Systems. Seckbach, J., and Oren, A. (eds). Dordrecht, The Netherlands: Springer, pp. 239-251.
28. Grissa, I., Vergnaud, G., and Pourcel, C. (2007a) The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinformatics 8: 172.
29. Grissa, I., Vergnaud, G., and Pourcel, C. (2007b) CRISPFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 35: W52-W57.
30. Guindon, S., and Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
31. Haft, D.H., Selengut, J., Mongodin, E.F., and Nelson, K.E. (2005) A guild of 45 CRISPR-associated (cas) protein families and multiple CRISPR/cas subtypes exist in prokaryotic genomes. PLoS Comput Biol 1: 474-483.
32. Heidelberg, J.F., Nelson, W.C., Schoenfeld, T., and Bhaya, D. (2009) Germ warfare in a microbial mat community: CRISPRs provide insights into the co-evolution of host and viral genomes. PLoS ONE 4: e4169.
33. Hendrix, R.W., Smith, M.C.M., Burns, R.N., Ford, M.E., and Hatfull, G.F. (1999) Evolutionary relationships among diverse bacteriophages and prophages: all the world's a phage. Proc Natl Acad Sci USA 96: 2192-2197.
34. Hoehler, T.M., Bebout, B.M., and Des Marais, D.J. (2001) The role of microbial mats in the production of reduced gases on the early earth. Nature 412: 324-327.
35. Horvath, P., and Barrangou, R. (2010) CRISPR/cas, the immune system of bacteria and archaea. Science 327: 167-170.
36. Hurwitz, B.L., and Sullivan, M.B. (2013) The pacific ocean virome (pov): a marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology. PLoS ONE 8: e57355.
37. Hurwitz, B.L., Hallam, S.J., and Sullivan, M.B. (2013) Metabolic reprogramming by viruses in the sunlit and dark ocean. Genome Biol 14: R123.
38. Hyatt, D., Chen, G.-L., LoCascio, P.F., Land, M.L., Larimer, F.W., and Hauser, L.J. (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11: 119.
39. Ignacio-Espinoza, J.C., and Sullivan, M.B. (2012) Phylogenomics of t4 cyanophages: lateral gene transfer in the 'core' and origins of host genes. Environ Microbiol 14: 2113-2126.
40. Karradt, A., Sobanski, J., Mattow, J., Lockau, W., and Baier, K. (2008) Nbla, a key protein of phycobilisome degradation, interacts with clpc, a hsp100 chaperone partner of a cyanobacterial clp protease. J Biol Chem 283: 32394-32403.
41. Kashtan, N., Roggensack, S.E., Rodrigue, S., Thompson, J.W., Biller, S.J., Coe, A., etal. (2014) Single-cell genomics reveals hundreds of coexisting subpopulations in wild prochlorococcus. Science 344: 416-420.
42. Kristensen, D.M., Waller, A.S., Yamada, T., Bork, P., Mushegian, A.R., and Koonin, E.V. (2013) Orthologous gene clusters and taxon signature genes for viruses of prokaryotes. J Bacteriol 195: 941-950.
43. Li, H., and Durbin, R. (2009) Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 25: 1754-1760.
44. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., etal. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
45. Lindell, D., Sullivan, M.B., Johnson, Z.I., Tolonen, A.C., Rohwer, F., and Chisholm, S.W. (2004) Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc Natl Acad Sci USA 101: 11013-11018.
46. Lindell, D., Jaffe, J.D., Johnson, Z.I., Church, G.M., and Chisholm, S.W. (2005) Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438: 86-89.
47. Litchman, E. (2000) Growth rates of phytoplankton under fluctuating light. Freshw Biol 44: 223-235.
48. Litchman, E., Steiner, D., and Bossard, P. (2003) Photosynthetic and growth responses of three freshwater algae to phosphorus limitation and daylength. Freshw Biol 48: 2141-2148.
49. Liu, X., Kong, S., Shi, M., Fu, L., Gao, Y., and An, C. (2008) Genomic analysis of freshwater cyanophage pf-wmp3 infecting cyanobacterium Phormidium foveolarum: the conserved elements for a phage. Microb Ecol 56: 671-680.
50. Luque, I., and Forchhammer, K. (2008) Nitrogen assimilation and c/n balance sensing. In The Cyanobacteria: Molecular Biology, Genomics, and Evolution. Herrero, A., and Flores, E. (eds). Norfolk, UK: Caister Academic Press, pp. 335-382.
51. Luque, I., Zabulon, G., Contreras, A., and Houmard, J. (2001) Convergence of two global transcriptional regulators on nitrogen induction of the stress-acclimation gene nbla in the Cyanobacterium synechococcus sp pcc 7942. Mol Microbiol 41: 937-947.
52. Ma, Y., Paulsen, I.T., and Palenik, B. (2012) Analysis of two marine metagenomes reveals the diversity of plasmids in oceanic environments. Environ Microbiol 14: 453-466.
53. Makarova, K.S., Grishin, N.V., Shabalina, S.A., Wolf, Y.I., and Koonin, E.V. (2006) A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol Direct 1: 7.
54. Makarova, K.S., Aravind, L., Wolf, Y.I., and Koonin, E.V. (2011a) Unification of cas protein families and a simple scenario for the origin and evolution of CRISPR-cas systems. Biol Direct 6: 38.
55. Makarova, K.S., Haft, D.H., Barrangou, R., Brouns, S.J.J., Charpentier, E., Horvath, P., etal. (2011b) Evolution and classification of the CRISPR-cas systems. Nat Rev Microbiol 9: 467-477.
56. Mann, N.H., Cook, A., Millard, A., Bailey, S., and Clokie, M. (2003) Marine ecosystems: bacterial photosynthesis genes in a virus. Nature 424: 741.
57. Middelboe, M. (2000) Bacterial growth rate and marine virus-host dynamics. Microb Ecol 40: 114-124.
58. Mizuno, C.M., Rodriguez-Valera, F., Kimes, N.E., and Ghai, R. (2013) Expanding the marine virosphere using metagenomics. PLoS Genet 9: e1003987.
59. Namiki, T., Hachiya, T., Tanaka, H., and Sakakibara, Y. (2012) MetaVelvet: an extension of velvet assembler to de novo metagenome assembly from short sequence reads. Nucleic Acids Res 40: e155.
60. van der Oost, J., Jore, M.M., Westra, E.R., Lundgren, M., and Brouns, S.J.J. (2009) CRISPR-based adaptive and heritable immunity in prokaryotes. Trends Biochem Sci 34: 401-407.
61. Paez-Espino, D., Morovic, W., Sun, C.L., Thomas, B.C., Ueda, K., Stahl, B., etal. (2013) Strong bias in the bacterial CRISPR elements that confer immunity to phage. Nat Commun 4: 1430.
62. Pride, D.T., and Schoenfeld, T. (2008) Genome signature analysis of thermal virus metagenomes reveals archaea and thermophilic signatures. BMC Genomics 9: 420.
63. Pride, D.T., Sun, C.L., Salzman, J., Rao, N., Loomer, P., Armitage, G.C., etal. (2011) Analysis of streptococcal CRISPRs from human saliva reveals substantial sequence diversity within and between subjects over time. Genome Res 21: 126-136.
64. Robinson, J.T., Thorvaldsdottir, H., Winckler, W., Guttman, M., Lander, E.S., Getz, G., and Mesirov, J.P. (2011) Integrative genomics viewer. Nat Biotechnol 29: 24-26.
65. Rodriguez-Valera, F., Martin-Cuadrado, A.-B., Rodriguez-Brito, B., Pasic, L., Thingstad, T.F., Rohwer, F., and Mira, A. (2009) Opinion: explaining microbial population genomics through phage predation. Nat Rev Microbiol 7: 828-836.
66. Ruberg, S.A., Kendall, S.T., Biddanda, B.A., Black, T., Nold, S.C., Lusardi, W.R., etal. (2008) Observations of the Middle Island Dinkhole in Lake Huron - a unique hydrogeologic and glacial creation of 400 million years. Mar Technol Soc J 42: 12-21.
67. Samson, J.E., Magadan, A.H., Sabri, M., and Moineau, S. (2013) Revenge of the phages: defeating bacterial defences. Nat Rev Microbiol 11: 675-687.
68. Sapranauskas, R., Gasiunas, G., Fremaux, C., Barrangou, R., Horvath, P., and Siksnys, V. (2011) The streptococcus thermophilus CRISPR/cas system provides immunity in Escherichia coli. Nucleic Acids Res 39: 9275-9282.
69. Sharon, I., Alperovitch, A., Rohwer, F., Haynes, M., Glaser, F., Atamna-Ismaeel, N., etal. (2009) Photosystem I gene cassettes are present in marine virus genomes. Nature 461: 258-262.
70. Shi, Y., Tyson, G.W., and DeLong, E.F. (2009) Metatranscriptomics reveals unique microbial small RNAs in the ocean's water column. Nature 459: 266-269.
71. Sorek, R., Kunin, V., and Hugenholtz, P. (2008) CRISPR - a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat Rev Microbiol 6: 181-186.
72. Stal, L.J. (2012) Cyanobacterial mats and stromatolites. In Ecology of Cyanobacteria II: Their Diversity in Space and Time. Whitton, B.A. (ed.). Heidelberg, Germany: Springer, pp. 65-125.
73. Sullivan, M.B., Lindell, D., Lee, J.A., Thompson, L.R., Bielawski, J.P., and Chisholm, S.W. (2006) Prevalence and evolution of core photosystem ii genes in marine cyanobacterial viruses and their hosts. PLoS Biol 4: e234.
74. Sun, C.L., Barrangou, R., Thomas, B.C., Horvath, P., Fremaux, C., and Banfield, J.F. (2013) Phage mutations in response to CRISPR diversification in a bacterial population. Environ Microbiol 15: 463-470.
75. Tadmor, A.D., Ottesen, E.A., Leadbetter, J.R., and Phillips, R. (2011) Probing individual environmental bacteria for viruses by using microfluidic digital PCR. Science 333: 58-62.
76. Thingstad, T.F. (2000) Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol Oceanogr 45: 1320-1328.
77. Tyson, G.W., and Banfield, J.F. (2008) Rapidly evolving CRISPRs implicated in acquired resistance of microorganisms to viruses. Environ Microbiol 10: 200-207.
78. 2: community genomics and function reveal metabolic versatility and extremely low diversity in a great lakes sinkhole mat. Geobiology 10: 250-267.
79. Weinbauer, M.G. (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28: 127-181.
80. Weinberger, A.D., Sun, C.L., Plucinski, M.M., Denef, V.J., Thomas, B.C., Horvath, P., etal. (2012) Persisting viral sequences shape microbial CRISPR-based immunity. PLoS Comput Biol 8: e1002475.
81. van der Westhuizen, A.J., and Eloff, J.N. (1985) Effect of temperature and light on the toxicity and growth of the blue-green alga Microcystis aeruginosa (UV-006). Planta 163: 55-59.
82. Yoshida, T., Nagasaki, K., Takashima, Y., Shirai, Y., Tomaru, Y., Takao, Y., etal. (2008) Ma-lmm01 infecting toxic Microcystis aeruginosa illuminates diverse cyanophage genome strategies. J Bacteriol 190: 1762-1772.
83. Yoshida-Takashima, Y., Yoshida, M., Ogata, H., Nagasaki, K., Hiroishi, S., and Yoshida, T. (2012) Cyanophage infection in the bloom-forming Cyanobacteria Microcystis aeruginosa in surface freshwater. Microbes Environ 27: 350-355.
84. Zerbino, D.R., and Birney, E. (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821-829.